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Rev Fish Biol Fisheries DOI 10.1007/s11160-012-9275-5

REVIEWS

Towards the conservation of freshwater fish: Iberian Rivers as an example of threats and management practices

Alberto Maceda-Veiga

Received: 28 February 2012 / Accepted: 25 June 2012 Ó Springer Science+Business Media B.V. 2012

Abstract The current freshwater fish fauna crisis is ecosystem researchers and stakeholders. Conservation such that natural resource managers urgently need to efforts should be focused on the preservation of identify priorities and understand the management ecological processes, in order to achieve the goals of consequences of actions aimed at maximizing the the Water Framework Directive and guarantee the preservation of biodiversity. Freshwater research is conservation of Iberian native fish species. often poorly linked to conservation ecology; and interdisciplinary studies illustrating examples of Keywords Aquatic conservation Á Management freshwater ecosystem conservation are scarce. The actions Á Endangered fish Á Freshwater Á Iberian Peninsula has a long history of anthropogenic Anthropogenic modifications disturbance that has led to the poor conservation status of its ichthyofauna, with 52 % of species now catalogued as critically endangered, endangered or vulnerable, according to UICN criteria. This paper gives an overview of the main threats (habitat Introduction degradation, hydrological alterations and exotic spe- cies) that have altered the function and connectivity of Freshwater ecosystems are some of the most threa- Iberian rivers. Case-study examples are provided to tened in the world. The loss of their biodiversity analyse the repercussions of these threats and the appears to be more intense than that of any other management actions planned or already performed in habitat (Dudgeon et al. 2006; Clavero et al. 2010; these systems. The interaction of many threats is Olden et al. 2010; Moyle et al. 2011). The number of responsible for native fish decline. However, fresh- endangered freshwater species on the International water managers and researchers should not let the Union for the Conservation of Nature (IUCN) Red List trees prevent them from seeing the overall wood, when has more than tripled since 2003 (Vie´ et al. 2009). This seeking to achieve practical solutions with the best concern is great in regions with a high degree of balanced cost benefit and the collaboration of all endemicity like the Mediterranean area in which 70 % of freshwater species are catalogued as threatened by extinction or are already extinct (Smith and Darwall A. Maceda-Veiga (&) 2005). This percentage is the highest recorded any- Department of Animal Biology (Vertebrates) and where in the world for any taxonomic group (Vie´ et al. Research Institute of Biodiversity (IRBio), Faculty of Biology, University of Barcelona, 08028 Barcelona, Spain 2009). Examples of freshwater fish decline and studies e-mail: [email protected] of population trends are common in the scientific 123 Author's personal copy

Rev Fish Biol Fisheries literature (Elvira 1995a, b; Aparicio et al. 2000; information provided may encourage researchers to Leprieur et al. 2008; Maceda-Veiga et al. 2010b; develop practical studies and help resource managers Moyle et al. 2011). Many of these studies have in the conservation of freshwater biota, especially in identified common causes of population decline areas with similar climatic conditions. (Elvira and Almodo´var 2001; Clavero et al. 2004; Nilsson et al. 2005; Dudgeon et al. 2006; Clavero et al. 2010; Gozlan et al. 2010; Olden et al. 2010; Hermoso Methods and Clavero 2011). The poor conservation status of Iberian freshwater fish species requires the design and Sources of information implementation of conservation plans (Filipe et al. 2004; Abell et al. 2007; Araguas et al. 2009; Nel et al. All native freshwater fish species from Iberia were 2009; Hermoso and Clavero 2011; Moyle et al. 2011; considered in the study, including anadromous and Olden et al. 2011). However, examples in the scientific catadromous species (e.g. Anguilla, Salmon, Alosa) literature of management action have long been biased and endemic species present in coastal lagoons (e.g. towards terrestrial ecosystems; research into freshwa- Aphanius, Valencia), but excluding amphidromous ter ecology is still not often linked to conservation species like mugilids. The IUCN Red List of ecology. Thus, interdisciplinary practical studies Threatened Species (www.iucnredlist.org) was used illustrating examples of freshwater fish conservation to compile information on the conservation status, are scarce (Lake et al. 2007; Nel et al. 2009; Strayer threats, population trends and conservation tools and Dudgeon 2010). required. This information, often used in similar Natural resource managers need to identify prior- studies (e.g. Clavero et al. 2010), was collected ities and understand the management consequences of through a regional assessment of fish endemic to the actions aimed at maximizing the preservation of Mediterranean basin by some 20 experts in fish biol- biodiversity (Dudgeon et al. 2006; Helfman 2007; ogy and conservation (Smith and Darwall 2005). Strayer and Dudgeon 2010; Olden et al. 2011; The examples used to illustrate potential or actual Grantham et al. 2012). Species decline may result management actions are based on reports and papers from the synergy of several impacts or from the identified via an intensive literature review, and by specific effect of one, whose proportional contribu- personal communication with freshwater managers tions to fish decline may also vary over time (Groom and researchers or with ecosystem stakeholders. The et al. 2006; Olden et al. 2010; Hermoso and Clavero main threats discussed are based on IUCN assessment 2011; Grantham et al. 2012). While large-scale and on the experience of researchers working on assessment can highlight the overall extent of the freshwater ecosystems, especially in regions with freshwater crisis, severity and causes are best under- similar climatic conditions (Doadrio 2001; Elvira and stood, even in large climatic areas (Hermoso and Almodo´var 2001; Sabater 2008; Sabater et al. 2009; Clavero 2011), by studies that focus on the regional Clavero et al. 2010, Elosegui et al. 2011; Hermoso and level (Moyle et al. 2011). The Iberian Peninsula Clavero 2011; Grantham et al. 2012). provides a suitable scenario for analysing the decline of freshwater fish because it has a high degree of fish endemicity and a long history of anthropogenic Conservation status of Iberian ichthyofauna disturbance (e.g. dams, forest exploitation, water extraction, extensive agriculture, water pollution, The conservation status of many species is critically industrialization, extensive forest fires, exotic intro- endangered, endangered or vulnerable. Populations ductions, fisheries) (Sabater et al. 2009; Clavero et al. are declining sharply, like freshwater ichthyofauna 2010; Hermoso et al. 2011; Maceda-Veiga and De elsewhere (Moyle et al. 2011; Hermoso and Clavero Sostoa 2011). This paper gives an overview of the 2011) (Fig. 1, Appendix 1). Freshwater fish diversity main threats to Iberian freshwater ichthyofauna. It in the Iberian Peninsula is characterised by a high shows the consequences that various management degree of endemicity (73 % of species are endemics to actions have had or may have on their conservation, the Iberian Peninsula) and restricted distribution using interdisciplinary case-study examples. The ranges (Fig. 2, Appendix 1). Exotic fish species 123 Author's personal copy

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the relative proportion of exotic species might be attenuated by the description of new native species (Kottelat and Freyhof 2007; Appendix 1).

Threats to freshwater biodiversity

According to UICN, the main threats to Iberian ichthyofauna are water extraction (including hydro- logical infrastructures) and introduced species, followed by climate constraints, pollution and over- exploitation (Table 1). These threats are shared with other Mediterranean regions (Hermoso and Clavero 2011). With a view to developing appropriate man- agement actions, the following subsections summarize how these and other reported threats to freshwater fish fauna in Iberia are affecting all key components of these freshwater ecosystems (i.e. riparian coverage, Fig. 1 Current conservation status of Iberian native fish species water flow level and quality, gravel bed streams and based on UICN criteria: CE critically endangered, E endangered, aquatic biota), together with the action of natural NT near threatened, V vulnerable, LC least concern and ND restrictions from the Mediterranean climate (i.e. forest without enough data fires and droughts). account for 42 % of Iberian freshwater fish, which is Hydrological infrastructures and water extraction similar to that reported for other European countries (Elvira 1995a, Doadrio 2001, Leprieur et al. 2008, Water extraction, considered one of the main threats Maceda-Veiga et al. 2010a, Appendix 2). However, to freshwater ecosystems worldwide, is a particular

Fig. 2 Population trends of the native freshwater fish fauna in Iberian Peninsula

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Table 1 Threats to Iberian native freshwater fish fauna and However, a multi-year study on the effects of drought proposed management actions based on IUCN criteria on Guadiana fish populations showed that in dry years % large barbels (Luciobarbus sclateri) and chub (Squa- lius torgalensis) declined, but small fish species like Impacts sticklebacks (Gasterosteus aculeatus) were favoured Water extraction 60.00 (Magalha˜es et al. 2007). No clear pattern has been Introduced species 50.00 reported for exotics (Leprieur et al. 2006; Boix et al. Climate change 48.33 2010). The susceptibility of fish to disease seems to Pollution 21.67 increase with supra-seasonal droughts (Maceda-Veiga Human exploitation 8.33 et al. 2009). Indeed, low fish abundance and specimens Urbanization 3.33 with a deteriorating body condition were found in Sau Management actions reservoir (Catalonia, NE of Spain) after a partial Habitat management 45.00 reservoir drawdown to optimize water quality for Habitat restoration 23.33 domestic demand (Benejam et al. 2010). Protected areas 16.67 The loss of river connectivity due to physical Species management 14.55 barriers affects long and short migratory species Ex-situ conservation 10.00 greatly (e.g. European eel, Anguilla anguilla; large Numbers shown are the percentage of species affected barbel species, Luciobarbus spp.; Atlantic salmon, Salmo salar) and has contributed to the almost confirmed extinction of some (e.g. Atlantic sturgeon, problem in arid and semi-arid regions such as the Acipenser sturio) (Elvira 1995a, b; Araujo and Ramos Mediterranean area (Sabater 2008; Boix et al. 2010; 2000; Smith and Darwall 2005). Examples of fish Clavero et al. 2010). The ratio water usage/availability species decline following damming are widespread in ranges from 4 to 7 % in northern Iberia to 80 % in the the literature (Almodo´var and Nicola 1999; Doadrio rest of the Peninsula, increasing from northwest to 2001; Gregory et al. 2002; Clavero et al. 2004). The southeast (i.e. from wet to arid regions) (Sabater et al. range of the European eel has declined by more than 2009). Excessive water extraction is particularly 70 % in north-eastern Spain (Maceda-Veiga et al. evident in the Tablas de Daimiel (Guadiana, Spain) 2010b), with a large decline also documented in other and many rivers in the Mediterranean area (Bromley European countries (Helfman 2007). The building of et al. 2001; Groom et al. 2006; Sabater et al. 2009). the main reservoirs was also responsible for the Many hydrological infrastructures were built in decline of the sea lamprey (Petromyzon marinus), 1960–1990 to satisfy agricultural, hydropower and sturgeon and shads (Alosa spp.) in the Guadalquivir domestic demand and to assist with flood regulation (Southern Spain) (Granado-Lorencio 1991), and the (Nicola et al. 1996; Almodo´var and Nicola 1999). almost extinction of the river lamprey (Lampetra These physical barriers (e.g. weirs, dams, channels) fluviatilis) in Tagus River (Perea et al. 2011). In cause hydrological alterations (e.g. flow regime, sed- contrast, some hydrological structures for agricultural iment trap), leading to irreversible alterations in river purposes (channels and farm pools) may also benefit function (e.g. hypersalinization of estuaries, sudden endangered native species that use them as a breeding water flow and temperature fluctuations), and directly refuge (e.g. river blenny, Salaria fluviatilis) (Aragon threaten aquatic biodiversity (e.g. restriction of migra- Forest Guard, personal communication). tion, destruction of spawning grounds, favouring inva- sions) (Almodo´var and Nicola 1999; Gregory et al. Introduction of non-native fish species 2002; Rovira and Iban˜ez 2007; Johnson et al. 2008). The effects of water flow reduction on fish popu- The Iberian Peninsula is a hotspot for exotic intro- lations are difficult to quantify because many abiotic ductions, considered a leading cause of extinctions and biotic interactions exist (Gasith and Resh 1999; (Leprieur et al. 2008; Clavero et al. 2010; Leunda Clavero et al. 2010). Small barbels (e.g. Barbus haasi) 2010). Nevertheless, analysis of the contribution of can survive in streams that retain isolated pools during exotic species to the decline of native species is often seasonal droughts (Aparicio and De Sostoa 1999). difficult because the former is concurrent with habitat 123 Author's personal copy

Rev Fish Biol Fisheries degradation (Didham et al. 2007). In this regard, bass, pike-perch) or forage/bait (e.g. bleak, roach) Hermoso et al. (2011) found that the abundance of (Elvira 1995a; Elvira and Almodo´var 2001; Leunda invasive species was the best single predictor of the 2010). Regardless of interconnections between water- decline of native species, regardless of their habitat courses, the use of native fish as bait/forage species is degradation status. Local extinctions of native fish associated with native translocations between Catalan have been recorded in the Mediterranean area without watersheds (Maceda-Veiga et al. 2010a). Trophic severe habitat degradation (Clavero et al. 2010). competition may appear with the translocation of Introduced species can replace native species through native species and the release of non-piscivorous trophic interactions, hybridization, behavioural inter- exotic fish (Gozlan et al. 2010; Cucherousset et al. actions or the transfer of diseases and pathogens 2011). For instance, an experimental assay illustrated (Leunda 2010). In addition, exotic introductions are that mosquitofish (Gambusia holbrooki) achieve responsible for alterations in ecosystem function (e.g. higher foraging values than the endangered fartet nutrient cycling) that may also lead to native species’ (Aphanius iberus) and samaruc (Valencia hispanica) decline (Leunda 2010). (Caiola and De Sostoa 2005).

Trophic interactions Hybridization

Predation is the most documented trophic interaction The co-habitation of similar genetic species may lead between native and introduced fish species. Although to hybridization between them. The release of brown the pattern is changing (Fig. 3), many exotic fish were trout (S. trutta) from hatchery stocks was common introduced into Iberian waters to satisfy the demands during the past century and continues to occur in of recreational fishing, either as predators (e.g. black Iberia. Iberian stocks originating in Germany and

Fig. 3 Changes in the origin of exotic fish species introduced into Iberian watersheds

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Rev Fish Biol Fisheries subsequent exchanges between hatcheries have aqueilognathi, Ichthyophthirius multifiliis), but there resulted in stocks with a high degree of genetic are undoubtedly many more that have not been homogeneity (Sanz and Pla 1998; Garcia-Marin et al. identified (Maceda-Veiga et al. 2009; Garcı´a-Berthou 1999). High levels of introgression were observed in et al. 2007; Gozlan et al. 2010). Up to 80 % (10) of the the heavily stocked Tajo and Mediterranean basins exotic parasites (12) found in Iberian fish are native to and the lowest level was reported in the Duero basin Asia (Garcı´a-Berthou et al. 2007; Maceda-Veiga et al. (Almodo´var et al. 2006). Thus, the strong genetic 2009). Of particular concern is the possible introduc- differentiation of native trout across Iberian drainage tion of Sphaerothecum destruens via the topmouth systems was lost, due to hatchery trout stocks gudgeon (Pseudorasbora parva), which is already (Almodo´var et al. 2006). In a similar way, the established in Iberia (Garcı´a-Berthou et al. 2007; translocation of native cyprinids between Iberian Gozlan et al. 2010). The potentially deleterious effects basins can lead to hybridization phenomena and loss of this intracellular parasite on native Iberian fish of fish diversity (Doadrio 2001). species have not been assessed, but the inhibition of reproduction of several European cyprinids (e.g. Behavioural interactions Leucaspius delineatus) is well documented (Gozlan et al. 2005). Fish and water transfers between basins Agonistic behaviour between native and introduced may also carry larvae or juveniles of other aquatic fish species has been poorly assessed (Caiola and De pests such as the zebra mussel (Dreissena polymor- Sostoa 2005; Alcaraz et al. 2008; Gozlan et al. 2010). pha) or the Asiatic clam (Corbicula fluminea), which Exotics may limit the use of particular habitats or food are already present in Iberia (Garcı´a-Berthou et al. sources by native species. An experimental assay 2007). using the native Ebro nase (Parachondrostoma miegii) and the exotic bleak (Alburnus alburnus) revealed that Alterations in nutrient cycling the bleak reduces the movement of the Ebro nase and that the former is the best trophic competitor in mixed Alterations of native fish communities can also impair co-habitation assays (Vinyoles et al. 2008). Another the ecosystem’s nutrient cycle (Gozlan et al. 2010) experimental assay found that native cyprinodontids (Fig. 4). The introduction of specialized plankton increased their defensive behaviour and captured more grazers (e.g. bleak) has a top-down effect on zoo- prey than the exotic mosquitofish (G. holbrooki)as plankton that results in the absence of cladocerans, salinity increased (Alcaraz et al. 2008). which are mainly responsible for the clear phase of lentic systems (Margalef 1983; Angeler et al. 2002). Transfer of diseases, pathogens and other pests As there are no specialist grazers of Iberian native fish species, plankton have evolved without this predation Exotic fish species may be vectors of pathogens that pressure. The introduction of these grazers has led to remain undetected until they cause clear symptomatic poor water quality in reservoirs and can increase costs fish diseases or mass mortality (Gozlan et al. 2005, of treatment for domestic demand (Vo¨ro¨smarty et al. 2010; Maceda-Veiga et al. 2009). Although fish 2010). Another example of alterations in nutrient disease is also a cause of population decline, the study cycling is related to the feeding activity of carp of its incidence in wild fish populations has received (Cyprinus carpio), which causes sediment resuspen- less attention than in commercial fish species (Garcı´a- sion with the consequent introduction of nutrients into Berthou et al. 2007; Maceda-Veiga et al. 2009; Gozlan the water column (Angeler et al. 2002; Gozlan et al. et al. 2010). For instance, the expanding eel trade in 2010; Cucherousset et al. 2011). This activity does not Asia has meant that the Asiatic nematode Anguillicol- have a clear top-down effect on zooplankton, but oides crassus is now widely distributed throughout resuspended sediment may damage the filter apparatus East Asia in Japanese eels but also in American of phytoplankton grazers, and the dissolved nutrients and European eels imported there to satisfy human favour algal blooms and the subsequent deterioration demand (Gozlan et al. 2010). Examples of exotic of water quality (Angeler et al. 2002). For instance, the parasite translocations already exist in Iberian presence of carp together with high temperatures may watersheds (e.g. Lernaea cyprinacea, Bothriocephalus have contributed to the bloom of the cyanobacteria 123 Author's personal copy

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Fig. 4 Effects of human activities and the burrowing activity of after increasing the dissolved nutrients and turbidity. Crossed- introduced species on a lake in terms of food web interactions. out arrows indicate the halted energy flow between Arrows indicate the energy flow within the aquatic ecosystem compartments

Plantktothrix rubescens in Vilasouto dam (Galicia, (Groom et al. 2006). Many of these pollutants present NW of Spain), with the consequent stoppage of the in sewage effluents are refractive to biological degra- water supply to nearby towns (Rodrı´guez, A., personal dation (e.g. metals, pesticides, herbicides, synthetic communication). hormones, drugs) and current sewage treatment plants fail to remove them (Lavado et al. 2004; Lavado 2006; Water pollution Musolff et al. 2010; Dama´sio et al. 2011). Some of these compounds also reach aquatic ecosystems by Most Iberian streams have been severely polluted by atmospheric deposition and run-off from adjacent industrial, agricultural and urban activities since the anthropic areas (i.e. diffuse pollution events) (Di mid twentieth-century (Sabater et al. 2009). The Giulo and Hinton 2008; Dama´sio et al. 2011). modernization of sewage treatment plants has sub- The uptake pathway and the effects that these stantially improved the chemical and biological qual- contaminants have on fish and ecosystems (e.g. ity of rivers in recent decades, even in low-flow bioaccumulation, biomagnifications) depend on many Mediterranean Rivers (Prat and Munne´ 2000; Maceda- factors that have been discussed elsewhere (e.g. life- Veiga et al. 2010a). Nevertheless, lethal fish spill history stage, trophic position of the organism, the events continue to occur in Iberia, even in protected type of xenobiotic) (Di Giulo and Hinton 2008). areas like the Natural Park of Sant Llorenc¸ (Catalonia, Examples of the effects of pollutants on fish inhabiting NE Spain) (Sostoa et al. 2007) or at Alnazco´llar, close Iberian freshwater ecosystems can also be found to Don˜ana National Park (Andalusia, Southern Spain) elsewhere (e.g. community structure alterations,

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Rev Fish Biol Fisheries physiological dysfunctions), but few studies have (Margalef 1983). The potentially toxic cyanobacteria focused on native fish species (Dama´sio et al. 2007; (e.g. Anabaena, Aphanizomenon, Microcystis, Nodu- Raldu´a et al. 2008), used biogeochemical tracers to laria and Planktothrix) are widespread in Spanish analyse ecosystem function (i.e. effects on ecological reservoirs and have dominated the phytoplankton processes) (Jardine et al. 2006) or used non-lethal community at least once in a high proportion of sampling (e.g. blood) (Maceda-Veiga et al. 2010b). investigated reservoirs (35–48 %) (Quesada et al. This is surprising, given the ethical questions involved 2004; Camargo and Alonso 2006). However, nutrient and the conservation status of many native species enrichment may also enhance phytobenthic biomass (Doadrio 2001; Maceda-Veiga et al. 2010a). The (Fig. 4), which may favour phytophagous and omniv- effects of pollution on such species remain unknown orous species like the Ebro nase (P. miegii) and the when exotics are used as sentinels because ecological Ebro chub (Squalius laietanus), respectively. and biological traits differ and determine the tolerance of species to anthropogenic stressors (Di Giulo and Fishery and aquaculture activities Hinton 2008; Maceda-Veiga and De Sostoa 2011). In addition, few studies exist on the effects of personal Inland fisheries are not directly a major threat in care products and drugs on aquatic organisms, even the Mediterranean basin, unlike other regions of the though this is now a worldwide concern, as many of world where freshwater fish are an important source these compounds act on biochemical pathways that are of protein (Hermoso and Clavero 2011). However, common among all vertebrates (i.e. these compounds excessive harvesting is contributing to the decline of affect humans and other vertebrates in a similar way) some prized recreational and commercial fish species (Musolff et al. 2010). (e.g. S. trutta, A. anguilla, P. marinus) and almost The input of excess nutrients from urban and caused the extinction of the Atlantic sturgeon (Doad- agricultural sewage discharges into watercourses rio 2001). Recreational fishing is more important (i.e. together with excessive pre-baiting (e.g. cereal mush it involves millions of people) than inland commercial release) in recreational fishing to attract cyprinids are fisheries and contributes substantial social and eco- leading causes of eutrophication (Arlinghaus et al. nomic benefits to local and national economies (e.g. 2002) (Fig. 4). Many studies have examined the fishing industries close to reservoirs) (Arlinghaus et al. effects of ammonia, nitrites and a vast range of 2002; Lewin et al. 2006). In the absence of official xenobiotics on aquatic species, but few have analysed records, the volume of captures and the contribution of the effects of nitrates on fish species, especially native this recreational fishing to the economy are difficult to Iberian fish species (Camargo 2005; Camargo and calculate (Cowx 2000; Arlinghaus et al. 2002). As Alonso 2006). The effects of nitrates have long been stated in the sections above, this activity is also the underestimated, but they limit blood oxygen transport main cause of fish introduction and has several other (i.e. haemoglobin oxidation) and cause endocrine dis- collateral effects on aquatic ecosystems (e.g. eutro- ruption in fish and amphibian populations (Camargo phication, introduction of bait and game species) and Alonso 2006; Edwards and Guillette 2007). (Lewin et al. 2006). Up to 19 % of groundwater and over 50 % of water Salmonid aquaculture is widespread in Iberia and stored in reservoirs are affected by eutrophication in deleterious effects on brown trout have already been Iberia (Sabater et al. 2009). Together with the decrease documented (i.e. genetic introgression), together with in water transparency, algal blooms may also be the introduction of exotic salmonid species is ( not a [e.g. responsible for oxygen depletion at night. The wide- rainbow trout, Onchorhynchus mykiss) due to escapes spread death of fish is probably the most dramatic (Elvira and Almodo´var 2001;Doadrio2001). Aquacul- manifestation of hypoxia (or anoxia) and the produc- ture research centres and ornamental aquaculture facil- tion of highly toxic compounds (e.g. hydrogen ities have also been responsible for the introduction of sulphide (H2S)) in eutrophic aquatic ecosystems exotic species (e.g. Mummichog (Fundulus heterocli- (Camargo and Alonso 2006). The proliferation of tus), Oriental Weather loach (Misgurnus anguillicaud- cyanobacteria is also of particular concern for fresh- atus), Topmouth gudgeon (P. parva)] in the Ebro Delta water managers because phytotoxins (i.e. microcys- (Catalonia, NE Spain). Environmental degradation tins) have repercussions on both human and fish health caused by effluent release or the spread of diseases 123 Author's personal copy

Rev Fish Biol Fisheries and pathogens (e.g. Gyrodactylus salaris, S. destruens) aquatic ecosystems and fish communities are lacking. in native populations is also possible (Arlinghaus et al. It causes physical obstructions to water flow, can cover 2002; Gozlan et al. 2010). the river bed during drought, contains lower arthropod diversity and evapotranspires three times more than Alteration of riparian coverage native riparian species (Coffman 2007). The periodic removal of riparian shading (e.g. Human settlements have existed along watercourses in logging trees, eradication of Giant reed) changes the Iberia from ancient times and riparian zones have been source of energy in the stretches affected from forest extensively deforested and converted to agricultural, inputs to primary producers present in the river (i.e. urban and industrial areas (Sabater et al. 2009). Fish algal biomass), which may result in substantial oxygen thus live in a mosaic of non-forested and forested areas depletion at night (Sabater 2008). Large unshaded with plantations of native and introduced species that areas may have a direct long-term effect on fish greatly affect river function (Naiman and De´camps populations. Studies of salmonids reported high mor- 1997; Elosegui et al. 2011). The ecological importance tality of eggs, embryos and larvae, and the appearance of riparian coverage by rivers and its direct effect on of cataracts in adult fish, after continuous exposure to fish are discussed in detail elsewhere. Riparian high but natural levels of solar UV-B (Helfman 2007). coverage is linked to the following: intercepting The loss of shading may also increase water temper- sediments, reducing erosion, acting as a green filter ature by up to 8 °C, which may exacerbate the effects (i.e. removing contaminants), controlling water tem- of climate change on aquatic ecosystems (Johnson and perature and filtering UV radiation, providing nutri- Jones 2000). Coldwater species, like the endangered ents and contributing to habitat diversification (Sagar Pyrenean sculpin (Cottus hispaniolensis) or the brown and Glova 1995; Naiman and De´camps 1997; Elosegui trout, which have a thermal range below 20 °C, will be et al. 2011; Flores et al. 2011). the most severely affected by such changes (Sostoa As well as affecting river function, large exotic 1990; Moyle et al. 2011). These extractive riparian plantations may also influence the supply of fish food. practices may also have other collateral effects on Indeed, tree cover may be less important than prey aquatic communities (e.g. increased run-off and availability in determining habitat choice by fish siltation, use of herbicides) (Beschta et al. 2004; (Sagar and Glova 1995). Extensive eucalyptus (Euca- Helfman 2007). lyptus globulus) and Monterrey pine (Pinus radiata) plantations in northwestern Iberia have changed the timing, quality (i.e. C:N:P ratio) and quantity of litter Forest fires input into streams. For instance, litter input from eucalyptus plantations occurs throughout the year, Forest fire is a natural phenomenon that can have great with a peak in summer, although the litter is less ecological, economic and sociological repercussions diverse and total input may be smaller and of lower (Otero et al. 2011; Pettit and Naiman 2007). The nutritional quality (lower N and P content) than in abandonment of forest and agricultural practices in native deciduous forests (Ferreira et al. 2006). This rural areas has led to an increase in fuel and fire risk in may have repercussions on invertebrate communities Iberia, mainly due to involuntary and/or criminal and fish productivity. In this regard, deciduous forest human actions (Otero et al. 2011). streams contain a greater diversity of invertebrates Fire may cause the following changes in aquatic than eucalyptus forest streams (Abelho and Grac¸a ecosystems: decreased stream channel stability, 1996; Ferreira et al. 2006). greater and more variable discharge, altered coarse Ruderal plant species like the Stinging Nettle woody debris delivery and storage, increased nutrient (Urtica dioica) or the elmleaf blackberry (Rubus availability, higher sediment delivery and transport, ulmifolius) have replaced native riparian coverage in increased solar radiation, altered water temperature areas with high anthropic impact. The invasive Giant regimes and the release of toxic compounds (e.g. flame reed (Arundo donax) has also colonized extensive retardants, polycyclic aromatic hydrocarbons) (Ri- riparian areas of Mediterranean rivers (Munne´ et al. eman and Clayton 1997; Dunham et al. 2003; Vila- 2003). Detailed studies on the effects of Giant reed on Escale´ et al. 2007; Raldu´a et al. 2008). The effects of 123 Author's personal copy

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fire on aquatic ecosystems may also depend on the and Light (1996), invasion by non-native fish is intensity of the fire itself, pre- and post-fire forest inevitable if the abiotic environment is suitable for management practices, natural climate constraints (i.e. their reproduction and growth. floods cause soil erosion and run-off into the river) and the presence of other anthropogenic pressures (e.g. Gravel extraction pollution events, weirs) that also constrain aquatic community resilience (Dunham et al. 2003; Sostoa Mining in gravel bed streams irreversibly disturbs the et al. 2003; Pettit and Naiman 2007). There is limited hydrological and ecological function of watersheds understanding of the short- and long-term effects of (e.g. silting, changes in river bank morphology and fire on fish, which makes assessment of the risks and pool availability), but its direct effects on fish popu- benefits of fire management practices pre- and post- lations are relatively unknown (e.g. Cote´ et al. 1999). fire difficult (Rieman and Clayton 1997; Dunham et al. There is much concern over this issue, as a decline in 2003; Raldu´a et al. 2008; Otero et al. 2011; Pettit and lithophilous species (e.g. nase) was documented in Naiman 2007). Switzerland after arid extraction (Zbinden and Maier The immediate consequence of a forest fire in the 1996) and Iberian ichthyofauna include many lith- Natural Park of Sant Llorenc¸ (Catalonia, NE Spain) ophilous spawners (e.g. brown trout, chub, barbels) was a reduction in fish abundance within the burnt (Doadrio 2001; Appendix 1). Concerns are heightened study area (Sostoa et al. 2003). The stocks of the two when such mining affects endangered species with native fish species (Western Mediterranean barbel, specific habitat requirements, such as the river blenny Barbus meridionalis; Ebro chub, S. laietanus) (S. fluviatilis) (Sostoa 1990). Gravel extraction may remained in the unburnt areas, but post-fire recoloni- reduce the suitability of the habitat for breeding (i.e. zation of fishless stretches had not occurred 4 years small stones), with egg production being more after the fire due to the existence of physical (i.e. strongly affected than nesting density (Cote´ et al. weirs) and chemical (i.e. pollution input) barriers 1999). Thus, the long-term viability of these fish (Sostoa et al. 2003). The resilience of native fish to fire populations could be endangered in the absence of any seems to increase when the fire affects larger inter- positive density-dependent effects on juvenile sur- connected systems and highly mobile species (e.g. vival. Fortunately however, S. fluviatilis shows a salmonids) (Rieman and Clayton 1997). In this regard, degree of habitat plasticity, which is seen in the small Iberian barbels have reduced mobility even existence of breeding populations in lakes, agricultural during the spawning season (Aparicio and De Sostoa pools and reservoirs (Doadrio 2001; author’s personal 1999). Local extirpation of native species with patchy observation). distribution and restricted habitat requirements was also documented in North American rivers (Dunham et al. 2003). Nevertheless, the native community was Management actions re-established within a year through the return of migratory individuals that were presumably outside European States are required to protect and restore all the system during the fire and related disturbances aquatic ecosystems with the aim of achieving good (Rieman and Clayton 1997; Dunham et al. 2003). ecological status by 2015 (European Commission In contrast, the number of introduced species in St. 2000). As common threats are affecting Iberian fish Llorenc¸ Natural Park dropped from five to one (i.e. species, economic resources for conservation purposes carp, C. carpio), which remained in downstream should be allocated to improve ecological processes stretches of the unburnt area (Sostoa et al. 2003). rather than the conservation of single species. How- Similarly, post-fire floods containing high levels of ever, the success of management actions requires good suspended sediment were responsible for the elimina- biological and ecological understanding of the rele- tion of the non-native brook trout (Salvelinus fonti- vant species. For instance, sedentary fish species like nalis) and rainbow trout (O. mykiss) in Arizona red-tailed barbels are likely to respond to local habitat (Dunham et al. 2003). However, the effect on exotic restoration. To contrast, spawning migratory species fish species is difficult to predict because humans may like trout or large barbel species will require the aid recolonization after fire. As suggested by Moyle restoration of residential habitats and longitudinal 123 Author's personal copy

Rev Fish Biol Fisheries connectivity between adult, spawning and larval (Fig. 5) (Poff and Allan 1995; Rieman and Clayton habitats, if populations are to recover (Lake et al. 1997; Araujo and Ramos 2000; Dunham et al. 2003). 2007). In any case, a domino effect (i.e. iterative Following the IUCN criteria, the management tools effects) often exists in aquatic ecosystems and a considered necessary to reverse the situation of Iberian targeted group of species (e.g. other fish, aquatic species include habitat management and restoration, mammals, birds) and several river compartments may the creation of protected areas and in situ and ex-situ be benefited after the removal of main pressures conservation plans for particular species (Table 1).

Fig. 5 Effects of several management actions on the aquatic ecosystem. The width of each box indicates which threats the management action will have evident positive (?)or negative (-) effects on

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Habitat management and restoration Best water management policies based on the reduction of water extraction (e.g. changing irrigation Hydrological infrastructures and water extraction methods) and water re-utilization are also needed. Such measures would avoid the construction of more Hydrological impoundments and water extractions are dams and the interconnection of waterways, with their the main factors responsible for river connectivity loss associated sociological and ecological repercussions in Iberian rivers (i.e. habitat fragmentation). Water (e.g. regional human troubles, translocation of native flow intermittency is expected to increase with climate species, spread of exotic species, diseases and patho- change due to the subsequent increase in human water gens); and to guarantee the dilution capacity of rivers demands (Vo¨ro¨smarty et al. 2010; Hermoso and and restore their longitudinal functionality (Prat and Clavero 2011). Hydrological impoundment removal Munne´ 2000; Bromley et al. 2001; Dudgeon et al. needs to be studied carefully because these physical 2006; Lewin et al. 2006; Johnson et al. 2008; Maceda- barriers also confine exotic populations (Leprieur et al. Veiga et al. 2010b;Vo¨ro¨smarty et al. 2010; Hermoso 2006). A dam removal often has high social and and Clavero 2011). The re-establishment of river political consequences and the subsequent restoration connectivity would have direct improvements on of native fish communities is not always guaranteed migratory fish species movements, with subsequent (Gregory et al. 2002; Johnson et al. 2008). Removal of repercussions on the whole ecosystem (i.e. transfer of physical barriers would be particularly useful in small energy along the watercourse) and collateral benefits tributaries with obsolete dams, in which pristine native to other species (i.e. dispersion of glochidia of some fish populations may persist (Aparicio et al. 2000; freshwater clams) (Araujo and Ramos 2000; Helfman Maceda-Veiga et al. 2010b). Fish passes can help fish 2007). The absence of A. sturio specimens from Iberia overcome these physical barriers (Nicola et al. 1996; for many years is a likely cause of the decline of the Elvira and Almodo´var 2001; Santos et al. 2002; giant pearl mussel Margarifiera auricularia (Araujo Helfman 2007). However, for instance, only 8 % of and Ramos 2000). River connectivity is also crucial obstacles in Catalonia (NE Spain) have fish passes and for the recolonization of fishless areas from donor there are doubts about the usefulness of their design, as populations after high-impact disturbance (e.g. forest there is about those installed in other Iberian water- fires, spills) (Nicola et al. 1996; Gregory et al. 2002; sheds (i.e. species-specific, low water flow, poor Helfman 2007; Olden et al. 2011). maintenance) (Ordeix et al. 2011). These fish ladders are suitable for small physical barriers, but not for Dealing with non-native species large dams (Nicola et al. 1996; Olden et al. 2011). In such cases, migratory species need to be transported Human involvement converts the introduction of via terrestrial transport (e.g. eels at the Belesar dam, exotic species into aquatic systems into a social, Galicia, NW of Spain) (Lo´pez-Ares, personal com- economic and sometimes unpredictable ecological munication) or fish lifts (e.g. the Limia basin in problem (Garcı´a-Berthou et al. 2007; Gozlan et al. Portugal) (Santos et al. 2002). Although these man- 2010; Cucherousset et al. 2011). Further studies are agement actions may assist in fish conservation, the needed to clarify the ecological processes involved in hydrological alterations remain. Experimental water invasions (e.g. trophic competition by combining and sediment releases would be the best management traditional gut content and stable isotope analyses) option for large dams to guarantee river function and to establish the incidence of diseases in wild (Rovira and Iban˜ez 2007). Flow discharges should be freshwater fish populations (Elvira and Almodo´var adjusted according to the life history of the species 2001; Garcı´a-Berthou 2007; Maceda-Veiga et al. present, rather than simply establishing some mini- 2009; Gozlan et al. 2010; Cucherousset et al. 2011). mum flow requirement (Helfman 2007; Hermoso and However, exotics may now have become key trophic Clavero 2011). This is particularly important in resources in some watersheds, and their disappearance Mediterranean Rivers, in which strong and unpredict- may affect the populations of other valuable species able hydrologic fluctuations occur naturally (Gasith (e.g. endangered mammals, birds) (Groom et al. 2006; and Resh 1999; Hermoso and Clavero 2011). Tablado et al. 2010).

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Complete eradication once exotics are established Prevention is the best way to avoid further intro- and widespread is a utopia and highly costly. Never- ductions into watersheds. Education programmes, theless, local exotic eradication plans have a more together with the banned exploitation of recognized balanced cost-success ratio and are particularly useful invaders, are key steps towards achieving this goal when they are applied in small areas of high conser- (Elvira and Almodo´var 2001; Helfman 2007; Olden vation value (Aparicio et al. 2000; Clavero et al. 2004; et al. 2010). For instance, people believe that Eastern Maceda-Veiga et al. 2010b). For instance, the local mosquitofish (G. holbrooki) is the best mosquito extirpation of carp (C. carpio) with rotenone (Legu- controller, although Aphanius genus show similar mineÒ) in two consecutive applications with 6 days predation rates (Homski et al. 1994). Biological lap (90 and 50 ppb, respectively) has already been control practices need caution because they often successful in Zon˜ar lagoon (Andalusia, Southern Spain), result in the introduction of new invaders (e.g. G. which is inhabited by Atherina boyeri (Ferna´ndez- holbrooki for mosquito control or grass carp, Cteno- Delgado 2007). After carp removal, water transparency pharyngodon idella, for vegetation control) (Elvira increased, macrophytes were also detected and diving and Almodo´var 2001; Gozlan et al. 2010). In addition, ducks [e.g. Common Pochard (Aythya ferina), White- some management practices planned to benefit native headed duck (Oxyura leucocephala) and Little Grebe species may threaten them by limiting trophic (Trachybaptus ruficollis)] returned to the lagoon. Prior resources at the larval and juvenile stages. Pyrenean to the treatment, the piscivorous Grey Heron (Ardea minnows (Phoxinus bigerri and similar species) are cinerea) and Great Cormorant (Phalacrocorax carbo) released into watercourses as a food supply to enhance dominated the water-bird community. To eradicate brown trout catches. However, the juvenile brown exotics in current waters, it seems more prudent to use trout (\20 cm) and the minnows, which form dense other methods such as successive electrofishing passes, shoals, both forage mainly on the same prey items (i.e. nets and traps. trophic competition) (Oscoz et al. 2008). Re-establishment of the natural hydrological The educational task is more difficult when exotics regime may also hinder the spread and establishment already enhance local or regional economies. For of exotic species (i.e. limnophilous species) in current instance, recreational fish industries adjacent to large waters (Poff and Allan 1995; Elvira and Almodo´var reservoirs or lakes are now fully developed for the 2001; Clavero et al. 2004; Maceda-Veiga et al. exploitation of exotic fish species, including fishing 2010b). Moyle and Light (1996) argued that the competitions (e.g. black bass in Ebro reservoirs). importance of biotic resistance to invasion is low when Current inland fisheries legislation needs to be applied environmental conditions favour exotics. Healthy evenly through all Iberian regions to face common native fish communities may resist invasion when issues like the introduction of exotic species (e.g. the introduced species are non-piscivorous because the euthanize and banned live-bait and pre-baiting activ- native species might use the natural resources present ities). In this regard, fisheries regulation, involving more efficiently (Gozlan et al. 2010). As Iberian fish restrictions on the number of captures and the species have evolved under low predation pressures, increased length of removed fish in Iberian water- they are especially vulnerable to exotic predator fish sheds, have had a certain amount of success in some species (Doadrio 2001; Elvira and Almodo´var 2001). native species like the brown trout (Almodo´var et al. Particular environmental conditions sometimes act as 2006; Araguas et al. 2009). It is also worthwhile a natural refuge for endangered species. In Spanish encouraging anglers to practice less invasive recrea- wetlands, mosquitofish peak at intermediate salinities tional fishing (e.g. catch-release practices), although and are rare in coastal lagoons with salinities[15 %, substantial post-release mortality and reduction in the where they are replaced by the Spanish toothcarp growth and fitness of released specimens have also A. iberus, which has mainly been extirpated from fresh been documented (Arlinghaus et al. 2002). and oligosaline waters (Alcaraz et al. 2008). Never- Together with angling activities, attention should theless, the recent introduction of another hyperhaline- be paid to aquaculture facilities (research, ornamental tolerant species, the mummichog (F. heteroclitus), is a and food) and releases of unwanted pets, because these new threat to A. iberus populations (Garcı´a-Berthou are emerging as important pathways for freshwater et al. 2007). introductions and have received minimal attention 123 Author's personal copy

Rev Fish Biol Fisheries from regulatory agencies (Olden et al. 2010; author authors suggested that the effluents from sewage unpublished data). Perhaps everyone who handles treatment plants should probably be maintained at a wild and captive fish (e.g. anglers, employees of dilution rate below 5 % of the total discharge of the ornamental fish stores) should receive training and receiving waters if healthy aquatic invertebrate have to obtain a permit for handling and/or selling assemblages are to be preserved. The role of river these species. To prevent further invasions, predictive pollution awareness is also relevant to the manage- models may also help managers to identify potential ment of effluents from sewage treatment plants. In invaders before they are introduced (Garcı´a-Berthou contrast to the cheapest location downstream from 2007). Thermal tolerance is a key parameter in these towns, citizens and local farmers are more conscious models that are region-specific (Garcı´a-Berthou of pollution events in rivers when sewage inputs are 2007). Special attention should be paid to regions placed upstream, and the subsequent social repercus- with a wide range of climatic conditions (i.e. north- sions affect water management decisions (Prat, per- western Iberia is colder than the south); and the effects sonal communication). The Ripoll river (Beso`s basin, of climate change, which will favour the introduction Catalonia, NE Spain), which was considered one of and spread of tropical species, should be taken into the most polluted rivers in Europe, benefited from account. these changes in the position of sewage inputs and partially recovered its native fish fauna in a short Water pollution period of time (2003–2007) (Sostoa et al. 2007). However, spills still occur and sub-lethal effects are Acute and diffuse water pollution are the main reasons evident in these fish species exposed to sewage for habitat degradation and, as stated above, their effluents (Maceda-Veiga et al. 2010b). The creation consequences are exacerbated in arid and semi-arid of adjacent lagoons connected to the main stream on ecosystems by the reduced capacity of rivers to dilute the downstream side could be an additional useful because of climatic and anthropic constraints (i.e. management action to guarantee fish survival in case water extractions) (Hermoso and Clavero 2011; of spills in these high-risk areas. Fish can swim to Grantham et al. 2012). Climate change could increase these refugee areas when they detect the presence of these deleterious effects on aquatic organisms because xenobiotics in the main river, and recolonize it after high water temperatures increase the metabolism of the water flow re-establishes the water quality. The poikilotherm organisms (e.g. fish) (Helfman 2007; recuperation of rivers’ water quality also has collateral Di Giulo and Hinton 2008). Diffuse water pollution effects. The nutrient reduction (especially phospho- can be reduced by encouraging farmers to be more rus) causes phytoplankton depletion with the subse- ecological or by introducing economic incentives to quent increase in water transparency in the lower Ebro persuade them to produce more ecological crops. The (Iban˜ez et al. 2008). In addition, hydrological regula- eradication of acute water pollutant events mainly tion has removed the effect of the natural shaping requires the removal of illegal collectors, making agents (i.e. flooding events) in Mediterranean rivers sewage treatment plants big enough to handle the input (Hermoso and Clavero 2011). The result is the flow of sewage and installing in these plants green spreading of macrophyte coverage and the annoying filters (i.e. tertiary treatment), through which effluents black fly (Iban˜ez et al. 2008). However, this scenario is can flow before reaching the river. However, these also likely to have increased the effects of predation on investments could be ineffective, in part, when the native estuarine species, because estuarine fish natural hydrological regime is not guaranteed and the evolved in turbid waters and now become more self-depuration of rivers is limited (e.g. deterioration visible to the large number of exotic predators present of riparian coverage), as is the case of Mediterranean in this basin (Helfman 2007; Maceda-Veiga et al. rivers (Prat and Munne´ 2000). 2010a). Measuring how waste water treatment plant efflu- ents affect aquatic communities based on river flow Riparian coverage and insights into forest fires has important implications for the way rivers are managed in Iberia and other Mediterranean climate Riparian coverage is a key component of freshwater regions of Europe (Grantham et al. 2012). These ecosystems (e.g. Naiman and De´camps 1997), but 123 Author's personal copy

Rev Fish Biol Fisheries important features of riparian forest ecology (e.g. important for the river in creating physical habitat and vigour of seedling growth, size- or age-distribution, recycling nutrients (Beschta et al. 2004; Elosegui et al. abundance of dead wood) are not properly assessed in 2011). An experimental assay in the Basque Country widely applied riparian quality indices (e.g. QBR) (Northern Spain) used this approach and reported a (Munne´ et al. 2003; Elosegui et al. 2011). The current low turnover of organic matter and an increase in abandonment of farming could be combated by invertebrate density and brown trout biomass and age- authorities giving economic incentives for forest classes (Flores et al. 2011; Elosegui et al. 2011). To restoration or directly performing the periodic clearing avoid excessive run-off of sediment into the river, of riparian and forest cover and the removal of exotics plantations of native riparian species and the installa- (i.e. Giant reed). This would reduce the evapotrans- tion of transverse physical barriers may also help to piration rate and the risk of forest fires, especially in stabilize the substrate prior to the recovery of riparian the Mediterranean area (Coffman 2007; Otero et al. coverage. However, the installation of complex bank 2011). These periodic activities clearing away the stabilizers alone may be limited in its efficacy, with riparian canopy should only affect short and staggered high costs and a short lifetime, especially in fast- stretches of stream, because major changes in aquatic flowing streams (Beschta et al. 2004). communities have been reported after the removal of as little as 150 m of riparian canopy (Elosegui et al. In situ and ex-situ conservation programmes 2011). Herbicides to eradicate exotic plantations should be used with caution. For Giant reed eradica- The strong decline of freshwater fish species implies tion, it was reported that an assay with the herbicide that further ex-situ conservation plans should be glyphosate in realistic concentrations caused certain implemented in the near future (Elvira 1995b; Doadrio oxidative stress and potentially genotoxic effects to 2001; Smith and Darwall 2005; Maceda-Veiga et al. the blood cells of a tolerant species like the European 2010a). Genetic reservoirs and captive breeding have eel in the Llobregat basin (Catalonia, NE Spain) been used for in situ conservation and to protect (Pue´rtolas et al. 2010; Maceda-Veiga and De Sostoa remnant populations of endangered species in ex-situ 2011). The removal of these exotic plantations should conservation programs, respectively (Groom et al. be followed by riparian restoration programmes. 2006; Araguas et al. 2009). Small endangered fish Riparian buffers with widths ranging from 5 to 30 m species are often candidates for ex-situ conservation have been found to be 50–75 % effective at preserving programs as they are easy to breed and maintain in the ecological functions of pristine forest streams in captivity (i.e. A. iberus, V. hispanica, G. aculeatus, Britain (Wichert and Rapport 1998). S. fluviatilis). The expert advice of highly qualified The best ecological option in regions with tradition aquarium hobbyists (e.g. Aquarium hobbyist associ- in forest plantations (e.g. North and NW Iberia) is to ations) may be helpful in this respect, although at keep riparian buffer strips of deciduous native vege- present such groups are generally ignored in fish tation mixed with these plantations to mitigate their conservation programmes (Escribano-Alacid, per- effect on the nutrient cycle by increasing the diversity sonal communication). of litter input into the streams (Abelho and Grac¸a A common strategy for the recovery of wild 1996; Ferreira et al. 2006). This forest structure populations involves the release of individuals from without large areas of pyrophilous species (e.g. Pinus, captive stocks or transfer from other healthy wild Eucalyptus, Arundo) may also diminish the risk of populations (Groom et al. 2006; Helfman 2007; Olden forest fires. However, it should not be forgotten that et al. 2011). Nevertheless, it would be more prudent to forest fires are a natural disturbance in Mediterranean try first to increase population size through habitat ecosystems. The possibility of recovery of burnt areas improvement and restrictive regulations for exploited is enhanced by leaving the burnt trees, whose deep and populations (e.g. trout) rather than to rely on reintro- extensive roots are much more effective than grasses duction or fish transfer from other populations (Sanz and shrubs at stabilizing stream banks. In addition, and Pla 1998; Groom et al. 2006; Olden et al. 2011). burnt trees and wood piles attract birds that, by Ex-situ conservation programs are controversial when dispersing plant seeds, assist the recovery of vegeta- reintroduction is unlikely. In addition, breeding native tion after fire (Rost et al. 2010). Dead wood is also species without genetic guarantees often leads to the 123 Author's personal copy

Rev Fish Biol Fisheries loss of diversity within populations, introgression and the Water Framework Directive and guarantee the eventually the extinction of local populations (Sanz conservation of Iberian native fish species. Native and Pla 1998; Araguas et al. 2009; Helfman 2007). ichthyofauna have suffered a strong decline in last The selection of an adequate number of breeding decades, but some small streams still maintain pristine individuals and consideration of the genetic peculiar- fish populations. In addition, freshwater ecosystems ities of each population are crucial in ex-situ conser- are recognized as systems open to rehabilitation vation breeding programs (Sanz and Pla 1998). In procedures. This means that fish and rivers themselves addition, captive-reared populations need to have can do most of the restoration work when the main sanitary guarantees and become familiar with condi- pressures disappear. In situ conservation measures tions in the wild before release (i.e. immunity need to be prioritized over the ex-situ ones. The best activation, being able to feed on wild prey, acquisition water management policies, together with the preser- of anti-predator behaviour) (Helfman 2007; Faria et al. vation of horizontal and longitudinal connectivity, are 2010). required in Iberian Rivers (in particular, in the The creation of ‘‘genetic refuges’’ and completely Mediterranean area) in order to preserve the ecosys- protected areas have aided in the conservation of tem function and maintain the ability of fish to native fish (Almodo´var et al. 2006). However, though recolonize fishless areas after natural or anthropic protected areas are little used in freshwater ecosystem catastrophes. Otherwise, natural constraints and protection, it is also worth noting that the removal of climate change may exacerbate the consequences of some impacts requires effective action at the basin current anthropogenic impact. In this context, climate scale and not just within a small protected area (Filipe change may increase the effects of water pollution on et al. 2004; Abell et al. 2007; Helfman 2007; Nel et al. aquatic ecosystems and favour the spreading of 2009). Genetic refuges, in which the release of tropical fish species in Iberia. Public awareness about hatchery fish is banned, have been established in the the threats posed by introduced species is required to eastern Pyrenees since 1997 by the Autonomous prevent further invasions. Despite the interaction of Government of Catalonia (NE Spain) as a manage- many threats to fish biodiversity, freshwater managers ment strategy to preserve the remaining native gene and researchers should not let the trees prevent them pools of brown trout and to improve fish catches from seeing the overall wood, when seeking to (Araguas et al. 2009). The collaboration of anglers’ achieve practical solutions with the best balanced cost associations has been crucial to extending these benefit. refuges to other river basins in the Pyrenees (Araguas et al. 2009). However, species recovery is sometimes Acknowledgments The author dedicates this manuscript to poorer than expected (Araguas et al. 2009) and his parents and thanks all those with whom he has had the opportunity to learn and talk about the conservation of sometimes high (Almodo´var et al. 2006). freshwater fish in Iberia, in particular Adolfo de Sostoa, Ignacio Doadrio, Carlos Ferna´ndez-Delgado, Jacint Nadal, Dolors Vinyoles, Emili Garcı´a-Berthou, Narcı´s Prat, Josep Concluding remarks Escribano-Alacid, Silvia Perea, Mario Monroy and the team of Forest Guards at Caspe (Arago´n). The career of AMV was supported by grants from ‘‘Xarxa de Refere`ncia en Aqu¨icultura The conservation of natural resources, including fish de la Generalitat de Catalunya’’ (Xraq), Catalan Water Agency, populations, is a social, political, economic and Ebro Water Confederation, Spanish Government and the ecological concern. Effective management actions Department of Animal Biology at the University of Barcelona. The author also thanked four anonymous referees for their require the understanding of all ecosystem stakehold- constructive review. ers and the application of an identical legislation evenly through all Spanish and Portugal regions to face common issues (e.g. exotic species). Conserva- Appendix 1 tion efforts should be focused on the preservation of ecological processes, in order to achieve the goals of See Table 2.

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Table 2 List and ecological guilds of native Iberian freshwater were extracted from the IUCN Red List of Threatened Species fish based on Doadrio 2001, Kottelat and Freyhof (2007) and (www.iucnredlist.org) in December 2011 Leunda et al. (2009). Conservation status and population trend Native fish species Status Spawning habitat Feeding habitat Trophic position Population trend

Achondrostoma arcasii V LITH WC OMNI Declining Achondrostoma occidentale E LITH WC OMNI Unknown Achondrostoma oligolepis LC LITH WC OMNI Unknown Achondrostoma salmantinum E LITH WC OMNI Declining Acipenser sturio CE – B INVE Declining Alosa alosa LC LITH WC PLAN Unknown Alosa fallax LC LITH WC PLAN Stable Anaecypris hispanica E PHYT WC OMNI Declining Anguilla anguilla CE – B PISC Declining Aphanius baeticus E PHYT WC INVE Declining Aphanius Iberus E PHYT WC INVE Declining Atherina boyeri LC PHYT WC INVE Unknown Barbatula quignardi LC LITH B INVE Unknown Luciobarbus bocagei LC LITH B OMNI Unknown Luciobarbus comizo V LITH B OMNI Declining Luciobarbus graellsii LC LITH B OMNI Unknown Barbus guiraonis V LITH B OMNI Declining Barbus haasi V LITH B INVE Declining Barbus meridionalis NT LITH B INVE Stable Luciobarbus microcephalus V LITH B OMNI Declining Luciobarbus sclateri LC LITH B OMNI Unknown Luciobarbus steindachneria V LITH B OMNI Declining Cobitis calderoni E LITH B INVE Declining Cobitis paludica V LITH B INVE Declining Cobitis vettonica E LITH B INVE Declining Cottus aturi LC LITH B INVE Unknown Cottus hispaniolensis LC LITH B INVE Unknown Gasterosteus aculeatusb LC PHYT WC INVE Unknown Gobio lozanoi LC LITH B INVE Unknown Iberochondrostoma almacai CE LITH B OMNI Declining Iberochondrostoma lemmingii V LITH B OMNI Declining Iberochondrostoma lusitanicum ND LITH B OMNI ND Iberochondrostoma olisiponensis ND LITH B OMNI ND Iberochondrostoma oretanum CE LITH B OMNI Declining Lampetra fluviatilis LC LITH B PLAN Unknown Lampetra planeri LC LITH B PLAN Unknown Parachondrostoma arrigonis CE LITH B PHYT Declining Parachondrostoma miegii LC LITH B PHYT Stable Parachondrostoma turiense E LITH B PHYT Declining Petromyzon marinus LC – B PISC Unknown Phoxinus bigerri LC LITH WC INVE Unknown Phoxinus septimaniaec LC LITH WC INVE Unknown Pseudochondrostoma duriense V LITH B OMNI Stable

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Table 2 continued Native fish species Status Spawning habitat Feeding habitat Trophic position Population trend

Pseudochondrostoma polylepis LC LITH B OMNI Stable Pseudochondrostoma willkommii V LITH B OMNI Declining Salaria fluviatilis LC LITH B INVE Stable Salmo salar LC LITH WC PISC Unknown Salmo trutta LC LITH WC PISC Unknown Squalius alburnoides complex V LITH B INVE Stable Squalius aradensis V LITH B OMNI Unknown Squalius carolitertii LC LITH B OMNI Unknown Squalius castellanus E LITH B OMNI Declining Squalius laietanus LC LITH B OMNI Unknown Squalius malacitanus E LITH B OMNI Declining Squalius palaciosi complex CE LITH B OMNI Declining Squalius pyrenaicus ND LITH B OMNI Declining Squalius torgalensis E LITH B OMNI Declining Squalius valentinus V LITH B OMNI Declining Syngnathus abaster LC – B INVE Unknown Tinca tinca LC PHYT B OMNI Unknown Valencia hispanica CE PHYT WC INVE Declining Conservation status categories: CE critically endangered, E endangered, V vulnerable, LC least concern, NT not threatened and ND nithout enough data for categorization; spawning habitat: LITH lithophilous and PHYT phytophilous; feeding habitat: WC water column and B benthic/benthopelagic; trophic position: PLAN planktophagous, INVE invertivorous, OMNI omnivorous and PISC piscivorous a This species is not valid for some authors who consider it an ecotype of Luciobarbus comizo with a hybrid origin. b The species Gasterosteus gymnurus is not supported by molecular data. c The existence of Spanish populations requires to be confirmed by genetic tools

Appendix 2

See Table 3.

Table 3 List of exotic fish Introduced fish species Status species introduced into Iberian catchments and Alburnus alburnus Invasive current status based on Doadrio (2001), Kottelat Ameiurus melas Invasive and Freyhof (2007), Leunda Australoheros facetus Invasive (2010) Carassius auratus Invasive Cyprinus carpio Invasive Fundulus heteroclitus Invasive Gambusia holbrooki Invasive Lepomis gibbosus Invasive Micropterus salmoides Invasive Misgurnus anguillicaudatus Invasive Pseudorasbora parva Invasive Sander lucioperca Invasive Silurus glanis Invasive

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Table 3 continued Introduced fish species Status

Abramis brama Naturalized Blicca bjoerkna Naturalized Esox lucius Naturalized Hucho hucho Naturalized Oncorhynchus kisutch Naturalized Oncorhynchus mykiss Naturalized Perca fluviatilis Naturalized Poecilia reticulata Naturalized Rutilus rutilus Naturalized Salvelinus fontinalis Naturalized Scardinius erythropthalmus Naturalized Acipenser baerii Uncertain Acipenser naccarii Uncertain Alburnoides bipunctatus Uncertain Aphanius fasciatus Uncertain Cobitis bilineata Uncertain Ictalurus punctatus Uncertain Lates calcarifer Uncertain Leuciscus idus Uncertain Astronotus ocellatus Unsuccessful Barbonymus schwanenfeldii Unsuccessful Ctenopharyngodon idella Unsuccessful Piaractus brachypomus Unsuccessful

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